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Topography of Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honeybee drone

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Summary

The endoplasmic reticulum (ER) in the photoreceptors of the honeybee drone, Apis mellifera, is highly differentiated and morphologically more complex than suggested by previous studies. In addition to the prominent voluminous submicrovillar cisternae we describe a submitochondrial ER. It separates the mitochondria-containing periphery from the core of the cell. The cell core contains many fenestrated ER cisternae that are horizontally and periodically arranged. We show that all parts of the ER, except for a tubulovesicular portion but including the nuclear envelope, are continuous; all parts appear to accumulate Ca2+ actively and with high affinity. Our results confirm previous suggestions that the submicrovillar ER is the major intracellular Ca2+ -store in the photoreceptors. The submitochondrial ER is thought to participate in Ca2+-regulation in the mitochondrial microenvironment. Moreover, we describe for the first time an extensive, morphologically complex Ca2+-sequestering ER in the pigmented glial cells; it might participate in the regulation of the glycogen metabolism.

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References

  • Berridge MJ (1987) Inositol trisphosphate and diacylgylcerol: two interacting second messengers. Ann Rev Biochem 56:159–193

    Google Scholar 

  • Bertrand D, Fuortes G, Muri R (1979) Pigment transformation and electrical responses in retinula cells of drone, Apis mellifera ♂. J Physiol 296:431–441

    Google Scholar 

  • Brown JE (1986) Calcium and light adaptation in invertebrate photoreceptors. In: Stieve H (ed) The molecular mechanism of photoreception. Springer, Berlin Heidelberg New York, pp 231–240

    Google Scholar 

  • Brown JE, Blinks JR (1974) Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. J Gen Physiol 64:643–665

    Google Scholar 

  • Campbell KP, Shamoo AE (1980) Phosphorylation of heavy sarcoplasmic reticulum vesicles: Identification and characterization of three phosphorylated enzymes. J Membr Biol 56:241–248

    Google Scholar 

  • Carafoli E (1987) Intracellular calcium homeostasis. Ann Rev Biochem 56:395–433

    Google Scholar 

  • Carsten ME, Reedy MK (1971) Cardiac sarcoplasmic reticulum: Chemical and electron microscope studies of calcium accumulation. J Ultrastruct Res 35:554–574

    Google Scholar 

  • Coles JA, Orkand RK (1985) Changes in sodium activity during light stimulation in photoreceptors, glia and extracellular space in drone retina. J Physiol 362:415–435

    Google Scholar 

  • Coles JA, Rick R (1985) An electron microprobe analysis of photo-receptors and outer pigment cells in the retina of the honeybee. J Comp Physiol 156:213–222

    Google Scholar 

  • Coles JA, Tsacopoulos M (1979) Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J Physiol 290:525–549

    Google Scholar 

  • Endo M, Iino M (1980) Specific perforation of muscle cell membranes with preserved SR functions by saponin treatment. J Muscle Res Cell Mot 1:89–100

    Google Scholar 

  • Fabiato A (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. In: Fleischer S, Fleischer B (eds) Methods of enzymology, Biomembranes 157, Academic press, Orlando, FL, pp 378–417

    Google Scholar 

  • Fahrenbach W (1969) The morphology of the eyes of Limulus: II. Ommatidia of the compound eye. Z Zellforsch 93:451–483

    Google Scholar 

  • Fein A, Tsacopoulos M (1988) Activation of mitochondrial oxidative metabolism by calcium ions in Limulus ventral photoreceptor. Nature 331:437–440

    Google Scholar 

  • Frixione E, Ruiz L (1988) Ca2+-uptake by smooth endoplasmic reticulum of peeled retinal photoreceptors of the crayfish. J Comp Physiol 162:91–100

    Google Scholar 

  • Horridge GA, Barnard PBT (1965) Movement of palisade in locust retinula cells when illuminated. Q J Microsc Sci 106:131–135

    Google Scholar 

  • Kirschfeld K, Vogt K (1980) Calcium ions and pigment migration in fly photoreceptors. Naturwissenschaften 67:516–517

    Google Scholar 

  • Kolb G, Autrum H (1972) Die Feinstruktur im Auge der Biene bei Hell- und Dunkeladaptation. J Comp Physiol 77:113–125

    Google Scholar 

  • Leskes A, Siekevitz P, Palade G (1971) Differentiation of endoplasmic reticulum in hepatocytes. I. Glucose-6-phosphatase distribution in situ. J Cell Biol 49:264–287

    Google Scholar 

  • Levy S, Fein A (1985) Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. J Gen Physiol 85:805–841

    Google Scholar 

  • Lieberman AR (1971) Microtubule-associated smooth endoplasmic reticulum in the frog's brain. Z Zellforsch 116:564–577

    Google Scholar 

  • Magalhaes MM, Coimbra A (1972) The rabbit retina Müller cell. A fine structural and cytochemical study. J Ultrastruct Res 39:310–326

    Google Scholar 

  • Margolis RN, Cardell RR, Curnow RT (1979) Association of glycogen synthase phosphatase and phosphorylase phosphatase activities with membranes of hepatic smooth endoplasmic reticulum. J Cell Biol 83:348–356

    Google Scholar 

  • Martin RE, Hafner GS (1986) Factors influencing the degradation of photoreceptor membrane in the crayfish, Procambarus clarkii. Cell Tissue Res 243:205–212

    Google Scholar 

  • McGraw CF, Somlyo AV, Blaustein MP (1980) Localization of calcium in presynaptic nerve terminals. J Cell Biol 85:228–241

    Google Scholar 

  • Minke B, Tsacopoulos M (1986) Eight induced sodium dependent accumulation of calcium and potassium in the extracellular space of bee retina. Vision Res 26:679–690

    Google Scholar 

  • Payne R (1987) Phototransduction by microvillar photoreceptors of invertebrates: mediation of a visual cascade by inositol trisphosphate. Photobiochem Photobiophys 13:373–397

    Google Scholar 

  • Payne R, Fein A (1987) Inositol 1,4,5 trisphosphate releases Ca2+ from specialized sides within Limulus photoreceptors. J Cell Biol 104:933–937

    Google Scholar 

  • Payne R, Walz B, Levy S, Fein A (1988) The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its control by negative feedback. Phil Trans R Soc London 320:359–379

    Google Scholar 

  • Peracchia C (1970) A system of parallel septa in crayfish nerve fibers. J Cell Biol 44:125–133

    Google Scholar 

  • Perrelet A (1970) The fine structure of the retina of the honey bee drone. Z Zellforsch 108:530–562

    Google Scholar 

  • Perrelet A, Bader CR (1978) Morphological evidence for calcium stores in photoreceptors of the honeybee drone retina. J Ultrastruct Res 63:237–243

    Google Scholar 

  • Skalska-Rakowska JM, Baumgartner B (1985) Longitudinal continuity of the subrhabdomeric cisternae in the photoreceptors of the compound eye of the drone. Experientia 41:43–45

    Google Scholar 

  • Somlyo AP (1984) Cellular site of calcium regulation. Nature 309:516–517

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    CAS  PubMed  Google Scholar 

  • Tsacopoulos M, Orkand RK, Coles JA, Levy S, Poitry S (1983) Oxygen uptake occurs faster than sodium pumping in bee retina after a light flash. Nature 301:604–606

    Google Scholar 

  • Tsacopoulos M, Coles JA, van de Werve G (1987) The supply of metabolic substrate from glia to photoreceptors in the retina of the honeybee drone. J Physiol Paris 82 (in press)

  • Ungar F, Piscopo I, Holtzman H (1981) Calcium accumulation in intracellular compartments of frog retinal photoreceptors. Brain Res 205:200–206

    Google Scholar 

  • Varela FG, Porter KR (1969) Fine structure of the visual system of the honeybee (Apis mellifera). J Ultrastruct Res 29:236–259

    Google Scholar 

  • Walz B (1979) Subcellular calcium localization and ATP-dependent Ca2+-uptake by smooth endoplasmic reticulum in an invertebrate photoreceptor cell. An ultrastructural, cytochemical and X-ray microanalytical study. Eur J Cell Biol 20:83–91

    Google Scholar 

  • Walz B (1982a) Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. I. Intracellular topography as revealed by OsFeCN staining and in situ Ca accumulation. J Cell Biol 93:839–848

    Google Scholar 

  • Walz B (1982b) Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements. J Cell Biol 93:849–859

    Google Scholar 

  • Walz B (1982c) Calcium-sequestering smooth endoplasmic reticulum in retinula cells of the blowfly. J Ultrastruct Res 81:240–248

    Google Scholar 

  • Walz B (1983) Association between cytoskeletal microtubules and Ca2+-sequestering smooth ER in Semper cells of fly ommatidia. Eur J Cell Biol 32:92–98

    Google Scholar 

  • Walz B (1985) Light-induced changes of extra- and intracellular potassium concentration in photoreceptors of the leech, Hirudo medicinalis. J Comp Physiol 157:199–210

    Google Scholar 

  • Walz B, Ziegler A, Baumann O (1988) Extracellular space (ECS) and endoplasmic reticulum (ER) as sources and sinks for Ca2+ mobilized by light in photoreceptors of the honeybee drone. In: Elsner E, Barth FG (eds) Sense organs. Thieme, Stuttgart New York, 209

    Google Scholar 

  • Whittle AC (1976) Reticular specializations in photoreceptors: a review. Zool Scripta 5:191–206

    Google Scholar 

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Authors and Affiliations

  1. Institut für Zoologie, Universität Regensburg, Regensburg, Germany

    O. Baumann & B. Walz

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  1. O. Baumann
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  2. B. Walz
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Baumann, O., Walz, B. Topography of Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honeybee drone. Cell Tissue Res. 255, 511–522 (1989). https://doi.org/10.1007/BF00218786

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